Hunting Tactics in a Cobweb Spider (Araneae-Theridiidae) and the Evolution of Behavioral Plasticity

Abstract

Although behavior is being gradually incorporated into phylogenetic studies, the understanding of the evolution of one of its main characteristics, plasticity or adjustment to environmental features, is still a challenge, mainly due to the lack of comparative data. In this paper we focus on the plasticity of the predatory repertoire of Achaearanea digitus, analyzing its responses to two prey types, and discuss the evolution of behavioral plasticity based on a comparison to the foraging repertoire of other araneoid sheetweavers and on a review of hunting tactics among the larger group of orbweavers. Contrasting with what was observed for other families, spiders of the family Theridiidae (among them A. digitus) show a small set of attack tactics, and a quite stereotyped predatory performance. These spiders regularly attack their prey with a typical sticky silk wrapping tactic, but fail to use other tactics such as bite–wrap or bite–pull out prey, which are commonly used in other spider families. We show that this stereotypy is typical of the foraging repertoire of araneoid sheetweavers. Plotting the mean size of the attack tactics repertoire on the phylogeny of Orbiculariae shows that high predatory stereotypy is a plesiomorphy of the whole araneoidea group, and that evolutionary increases in plasticity occur independently two times in the group, among Araneidae and Nephilidae. The maintenance of a plesiomorphic, stereotyped predatory behavior among theridiids is probably due to the evolution of a special behavioral technique, which includes the simultaneous use of the fourth legs during wrapping attacks. Since the individuals in the species of this group of sheetweavers face less variable environments than do orbweavers, they should indeed evolve more stereotyped phenotypes, but nevertheless their evolved predatory stereotypy contrasts with plasticity in other aspects of their foraging behavior (web building). Since, in this case, both stereotypy and plasticity result from a simplification in the mechanisms underlying behavioral expression, we suggest that less variable environments select not exactly for behavioral stereotypy, but rather to the simplification of these information processing mechanisms.

Appendix

Behavioral categories employed in the description of capture sequences

Category names are in italics. Categories followed by a symbol are significantly and positively associated to fixR (•), tug (), or wrap (*), the three categories which most contribute to the differentiation between the capture of beetle larvae and ants.

Approach: spider displacements towards the prey, without tensing the threads with the first pair of legs (see tug bellow). It occurs during the detection phase and is usually followed by prey-touching or prey-wrapping movements. Viera (1986) describes a similar category, “desplazamiento 2”, but her description encompasses both approaching and tugging movements.

Bite• (Robinson and Olazarri 1971): the spider extends the distal segments of the chelicerae and flexes one segment against the other onto the prey, touching or penetrating it for a long time. Viera (1986) divides the observed bites for Metepeira sp. in long, sustained insertions (during at least 20 s) and short, subtle insertions of chelicerae onto prey. In this paper we did not consider this distinction.

Carry on silk * (Robinson and Olazarri 1971): after the spider attached a thread onto the wrapped prey, she moves toward the retreat, carrying the prey behind it, held by the spinnerets or by one of the posterior legs (leg IV). Robinson and Mirick 1971 (see also Robinson and Olazarri 1971, Robinson and Robinson 1973) describe another category, carry on jaws, carried out by large spiders usually when preying upon small prey items; this category does not seem to occur among theridiids.

Cut thread (Robinson and Olazarri 1971): the spider cuts the threads either with her legs or chelicerae. She can cut the lines enveloping the prey, the lines connecting the prey to the web or the web lines.

Fix•* (Viera 1994): the spider moves her abdomen ventrally, touching the web or prey with the spinnerets, attaches a thread and leaves a new silk strand.

Fix and rotate (fixR; Robinson and Olazarri 1971; Viera 1994): after attaching the wrapped prey to the retreat, the spider turns to assume a head-down posture. During the turning process, the spinnerets are dabbed against the web in an arc. This sequence of web fixations during the turning process is named fixR. Peters (1931, apud Robinson and Olazarri 1971) describes this same movement (which he called Rundgang) for Araneus diadematus Clerk 1757.

Grooming (Robinson and Olazarri 1971): the spider rubs the appendages one against the other or against the spinnerets and/or abdomen. She also makes chewing movements with the chelicerae while passing slowly the tarsi of the appendages, one by one, between the chelicerae. She can also rub one chelicerae against the other.

Grope: at the retreat, the spider searches for the prey that is packed, hanging nearby on a thread. She tenses some of the web threads with legs I before she moves in the right direction (see retrieve below). This tensing looks like a tugging (see below), but is more subtle and occurs only after prey immobilization.

Manipulate•* (Robinson and Olazarri 1971): repeated touches on the body of the prey, with palps, legs or chelicerae, turning the prey package around and delivering short bites at various regions. In the present paper we excluded these short bites from manipulation.

Pause (Viera 1994): the spider halts at any moment of capture sequence and stands immobile (not withdrawn, see below) during 30 s or more.

Pay out a line• (Japyassú and Macagnan 2004, Garcia and Japyassú 2005): the spider attaches a thread to or nearby the wrapped prey and moves towards the retreat, leaving behind a dragline. As a variation of this category, the spider can stop a wrapping bout and move towards the retreat, leaving a new dragline without previously attaching the thread to the prey.

Reel (Japyassú and Macagnan 2004, Garcia and Japyassú 2005): usually at the retreat, the spider pulls the gumfoot line with her front legs (legs I, occasionally also with legs II), thus bringing the prey adhered to the gumfoot bellow towards herself. The spider first extends one leg I, grabs the gumfoot line and flexes the leg. She then alternates these same movements with both legs I, thus bringing the prey towards herself. The spider can occasionally extend and/or flex both legs at the same time. Ades (1972) describes a similar behavior (lifting, also named retrieve by Japyassú and Viera 2002). Although topologically similar, these behaviors occur in completely different contexts: reeling occurs before the contact with prey, during the detection phase, and lifting occurs long after prey immobilization, when the spider is at the retreat or hub and the prey is packed, hanging on a nearby thread.

Retrieve• (Japyassú and Macagnan 2004, Garcia and Japyassú 2005): usually at the retreat, the spider moves towards the wrapped prey that is hanging nearby on a thread or entangled at the periphery of the web. Viera (1994) describes a similar category (recuperación), but in this description the spider pulls the wrapped package towards her using legs I and II, instead of moving towards the prey. Although the result is the same (the spider touches the prey), the topology of the movement is very distinct. Retrieve is very usual and widespread among theridiids, but is rare among orbweavers.

Return • : the spider moves towards the retreat without leaving a dragline behind. This can occur before a sticky silk wrapping bout (see wrap below), usually when the spider fails to hit the prey.

Tug (Jackson and Brassington 1987): at the retreat, the spider moves legs I medially, while grasping silk lines with the leg tarsi. She holds the lines tensed for 1–2 s then relaxes its legs, returning to the normal position. The spider usually moves towards the prey before tensing the threads with legs I. She also tugs consecutively nearby gumfoot lines before reeling (see reel above) one of them.

Withdraw (Lubin 1980): Lubin observed this behavior in four species of Cyrtophora. She describes it as a cryptic position that involves pulling all the legs inward towards the body, thereby obscuring the typical spider-like outline.

Wrap (Robinson and Olazarri 1971): after reeling the prey, or after approaching and/or touching it, the spider throws dry (wrap) or viscid (sswrap) silk onto it, with alternate movements of legs IV, which repeatedly touch the spinnerets and move towards the prey. While legs IV cast silk, legs III hold the prey and the other legs hold web lines. The topology of these movements in A. digitus is similar to the one described for the orbweavers of the family Araneidae, and even for the unrelated spiders of the family Pholcidae (see Jackson and Brassington 1987, Japyassú and Macagnan 2004), but it is strikingly different from the one observed for Euryopis funebris (Hentz 1850), another theridiid (see Carico 1978). In an alternative, special wrapping technique, sswrap can be iniciated with simultaneous movements of legs IV, from the spinnerets to the prey: the spider first takes a thread (coated with viscid blobs) with the tip of one leg IV and then extends this leg laterally; next she grips this same line with the other leg IV and, with both legs, throws over the prey the viscid segment that is between her legs (Japyassú and Jotta 2005); these movements are repeated many times in a single wrapping bout. We have not observed the “bobbin like” wrapping that Robinson and Olazarri described for Argiope argentata (Fabricius 1775).